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  • Article | DOI: 10.21307/jofnem-2020-097
  • e2020-97 | Vol. 52

D e s c r i p t i o n o f H e t e r o d e r a m i c r o u l a e s p . n . ( N e m a t o d a : H e t e r o d e r i n a e ) f r o m C h i n a  a n e w c y s t n e m a t o d e i n t h e G o e t t i n g i a n a g r o u p

Wenhao Li1, Huixia Li1,*, Chunhui Ni1, Deliang Peng2,

Abstract

Yonggang Liu3, Ning Luo1 and Xuefen Xu1
A new cyst-forming nematode, Heterodera microulae sp. n., was

isolated from the roots and rhizosphere soil of Microula sikkimensis in China. Morphologically, the new species is characterized by lemon-shaped body with an extruded neck and obtuse vulval cone. The vulval cone of the new species appeared to be ambifenestrate without bullae and a weak underbridge. The second-stage juveniles have a longer body length with four lateral lines, strong stylets with rounded and flat stylet knobs, tail with a comparatively longer hyaline area, and a sharp terminus. The phylogenetic analyses based on ITS-rDNA, D2-D3 of 28S rDNA, and COI sequences revealed that the new species formed a separate clade from other Heterodera species in Goettingiana group, which further support the unique status of H. microulae sp. n. Therefore, it is described herein as a new species of genus Heterodera; additionally, the present study provided the first record of Goettingiana group in Gansu Province, China.
1College of Plant Protection, Gansu Agricultural University/Biocontrol Engineering Laboratory of Crop Diseases and Pests of Gansu Province, Lanzhou, 730070, Gansu Province, China.

2State Key Laboratory for Biology of Plant Diseases and Insect Pests, Institute of Plant Protection, Chinese Academy of Agricultural Sciences, Beijing, 100193, China.

3Institute of Plant Protection, Gansu Academy of Agricultural Sciences, Lanzhou, 730070, Gansu Province, China.

Keywords

Goettingiana group, Heterodera, Morphology, New species, Phylogeny,
*E-mail: [email protected]

Taxonomy.
This paper was edited by

Thomas Powers.

Received for publication July 5, 2020.

Cyst-forming nematodes are the economical pests of cultivated crops and known to be reported from all the continents (Jones et al., 2013). The genus Heterodera was erected by Schmidt (1871) and currently contains about 80 species (Subbotin et al., 2010). Literature studies have indicated the presence of 14 Heterodera species from China mainland, including H. avenae (Chen et al., 1991), H. glycines (Liu et al., 1994), H. sinensis (Chen and Zheng, 1994), H. filipjevi (Li et al., 2010), H. koreana (Wang et al., 2012; Wang et al., 2012b), H. elachista (Ding et al., 2012), H. ripae (Wang et al., 2012a; Wang et al., 2012b), H. hainanensis (Zhuo et al., 2013), H. fengi (Wang et al., 2013),

H. guangdongensis (Zhuo et al., 2014), H. zeae

(Wu et al., 2017), H. sojae (Zhen et al., 2018), H. schachtii, and H. vallicola (Peng et al., 2020).
Due to overlapping morphological characters and phenotypic plasticity, it is difficult to distinguish closely related Heterodera species; therefore, sequence-based diagnosis is gaining more reliability for precise and accurate identification of cystforming nematodes (Peng et al., 2003). The internal transcribed spacer region of the ribosomal DNA (ITS-rDNA), the D2 and D3 expansion fragments of the 28S ribosomal DNA genes (D2-D3 of 28S-rDNA), and mitochondrial DNA (COI gene) units are good candidate genes for molecular taxonomic and phylogenetic studies (Subbotin et al., 2001; Subbotin et al., 2006; Madani et al., 2004; Vovlas et al., 2017). Based on morphomolecular characterizations, Handoo and Subbotin (2018) divided Heterodera into nine distinct groups such as Afenestrata, Avenae,

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© 2020 Authors. This is an Open Access article licensed under the Creative Commons CC BY 4.0 license, https://creativecommons.org/licenses/by/4.0/

H e t e r o d e r a m i c r o u l a e s p . n . f r o m C h i n a : L i e t a l .

Bifenestra, Cardiolata, Cyperi, Goettingiana, Humuli,

Sacchari, and Schachtii group. Sequence analysis of these groups is significant to study the phylogenetic relationship and identifying the Heterodera species.
During 2018 and 2019, a population of cyst nematode was collected from the rhizosphere of Microula sikkimensis in Tianzhu county of Gansu Province, China. Considering the economic value of the cyst nematode, morphomolecular studies were performed; the preliminary studies indicated that the population belongs to Goettingiana group of Heterodera. The species characters were then compared with all the related species and concluded that this population possess unique characters and it is described herein as Heterodera microulae sp. n.
The 28S D2-D3 region was amplified with the D2A (5′-ACAAGTACCGTGAGGGAAAGTTG-3′) and D3B (5′-TCGGAAGGAACCAGCTACTA-3′) (De Ley et al., 2005; Ye et al., 2007). Finally, the partial COI gene was amplified using primers Het-coxiF (5′-TAGTT GATCGTAATTTTAATGG-3′) and Het-coxiR (5′-CCT AAAACATAATGAAAATGWGC-3′) (Subbotin, 2015). PCR conditions were as described by Ye et al. (2007), De Ley et al. (2005), and Subbotin (2015). PCR products were separated on 1% agarose gels and visualized by staining with ethidium bromide. PCR products of sufficiently high quality were purified for cloning and sequencing by Tsingke Biotech Co. Ltd., Xi’an, China. The PCR products were purified by the Tiangen Gel Extraction Kit (Tiangen Biotech Co. Ltd., Beijing, China), cloned into pMD18-T vectors and transformed into DH5α-competent cells, and then sequenced by Tsingke Biotech Co. Ltd (Xi’an, China).

Materials and methods

Isolation and morphological observation of nematodes
Sequence alignment and phylogenetic analysis

The nematodes were extracted from root and soil samples of Microula sikkimensis in Tianzhu county, Gansu Province, China. Cysts and white females were collected using sieving-decanting method, while second-stage juveniles (J2s) were recovered from hatched eggs and kept in water suspension until further use (Hooper, 1970; Golden, 1990). Males were not found. For morphometric studies, second-stage juveniles were killed by gentle heating, fixed in TAF solution (formalin: triethanolamine: water=7:2:91), and processed to ethanol-glycerin dehydration according to Seinhorst (1959) as modified by De Grisse (1969) and mounted on permanent slides. Vulval cones were mostly mounted in glycerin jelly. Measurements were made on mounted specimens using a Nikon Eclipse E100 Microscope (Nikon, Tokyo, Japan). Light micrographs and illustrations were produced using a Zeiss Axio Scope A1 microscope (Zeiss, Jena, Germany) equipped with an AxioCam 105 color camera and Nikon YS 100 with a drawing tube (Nikon, Tokyo, Japan), respectively.
The newly obtained sequences for each gene (ITS- rDNA, D2-D3 region of 28S-rDNA, and COI gene) were compared with known sequences of Heterodera using BLASTn homology search program. Outgroup taxa for phylogenetic analyses were selected based on the previously published studies (Subbotin et al., 2001; Maafi et al., 2003; Mundo-Ocampo et al., 2008; Kang et al., 2016; Madani et al., 2018; Vovlas et al., 2017). The selected sequences were aligned by MAFFT (Kazutaka and Standley, 2013) with default parameters and edited using Gblock (Castresana, 2000). Phylogenetic analyses were based on Bayesian inference (BI) using MrBayes 3.1.2 (Huelsenbeck and Ronquist, 2001). The GTR+I+G model was selected as the best-fit model of DNA evolution for both 28S D2-D3, ITS, and COI regions using MrModeltest version 2.3 (Nylander, 2004), according to the Akaike information criterion (AIC). BI analysis for each gene was initiated with a random starting tree and run with four Markov chains for 1,000,000 generations. The Markov chains were sampled at intervals of 100 generations and the burn-in value was 25%. Two runs were performed for each analysis. After discarding burn-in samples, the remaining samples were used to generate a 50% majority-rule consensus tree. Posterior probabilities (PP) were given on appropriate clades. The phylogenetic consensus trees were visualized using FigTree v.1.4.3 software (http://tree. bio.ed.ac.uk/software/figtree/) (Rambaut, 2016). The species in Goettingiana group and their localities, hosts, and GenBank accession numbers used in this study were presented in Table S1.

Molecular analyses

DNA samples were prepared according to Maria et al. (2018). Three sets of primers (synthesized by Tsingke Biotech Co. Ltd., Xi’an, China) were used in the PCR analyses to amplify sequences of the ITS, D2-D3 expansion segments of 28S, and COI gene. The ITS region was amplified with TW81 (5′-GTTTCCGTAGGTGAACCTGC-3′) and AB28 (5′-AT ATGCTTAAGTTCAGCGGGT-3′) (Maafi et al., 2003).

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brown; remnants of the subcrystalline layer were rarely present. The egg sac was usually absent (Figs. 1G, 3B, C). The vulval cone was ambifenestrate-like waning crescent moon and separated by a well-developed vulval bridge. The anus area was distinct, bullae were absent (Figs. 1F, 3D, E). The vulval slit was longer than fenestral width (39.00 vs 37.75µm); the underbridge was weak and often lost during cone preparation.

Results

Systematics

Heterodera microulae sp. n. (Figures 1–4; Measurement Table 1)

Description Cyst
Female

It is lemon-shaped with an obtuse vulval cone, neck extruding, and cuticle thick with an irregular zig-zag pattern. The color was white to pale to medium
The female was lemon-shaped, pearl white, or pale yellow in color. It was rarely rounded with a protruding

Figure 1: Line drawing of H. microulae sp. n. A: Anterior region of second-stage juvenile; B: Head of second-stage juvenile; C: Stylet of second-stage juvenile; D: Tail of second-stage juvenile; E: Cyst; F: Fenestration in vulval cone.

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Figure 2: Light micrographs of H. microulae sp. n. A: females attached on M. sikkimensis; B: yellow and white females; C: Anterior region of female; D: Vulval region of female (scale bar: A=2mm; B=1mm; C, D=20µm).

neck and vulva, the subcrystalline layer was present, and the egg sac absent (Figs. 2A, B, 3A). There was a labial region with two annuli. Labial sclerotization was weak, the stylet was strong, and basal knobs were rounded and anteriorly flattened. The excretory pore was indistinct, median bulb was rounded and

Figure 3: Light micrographs of H. microulae sp. n. A: immature female on the root; B: Cyst; C: Cysts; D-E: Fenestration in vulval cone; F: Egg (scale bar: A, D=50µm; B=100µm; C=200µm; E, F=20µm).

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Figure 4: Light micrographs of second-stage juvenile of H. microulae sp. n. A: Entire body; B: Anterior region of; C: Head region; D: Tail region; E: Posterior pharyngeal region arrow showing the position of dorsal gland nucleus; F: Posterior pharyngeal region arrow showing the position of subventral gland nuclei; G: Lateral field; H: Hemizonid; I: Genital primordium; J: Excretory pore (scale bar: A=100µm, B, H, G=50µm, C, D, E, F, I, J=20µm).

massive, and other parts of the pharynx were not clearly discernable. There was vulval slit in a cleft on the cone terminus (Fig. 2C, D). nucleus and subventral gland nuclei were distinct (Fig. 4E, F). Genital primordium situated at 59 to 62% of body length behind the anterior end, with two distinct nucleate cells (Fig. 4I). The tail was conoid, gradually tapering to a finely rounded terminus. The hyaline portion was irregularly annulated occupying 50% of tail length. Phasmid was absent (Figs. 1E, 4D).

Second-stage juvenile

The body was straight or slightly curved ventrally after heat treatment (Fig. 4A). The lip region was offset and rounded, measuring 3.90 to 5.50 (4.63) µm in height and 9.65 to 12.75 (11.01)-µm wide. The cephalic framework was strongly sclerotized (Figs. 1B, 4C). The stylet was strong; knobs were well developed, rounded and flat, or slightly concave anteriorly (Figs. 1C, 4C). The dorsal esophageal gland orifice measured from 5.32 to 6.32 (5.61) µm posterior to the stylet knob. Median bulb was rounded with a strong valvular apparatus. The pharyngeal glands were well developed, overlapping the intestine dorsoventrally (Figs. 1A, 4B). The hemizoind was distinct from one to three annuli long (Fig. 4H), the excretory pore was situated 102.46 to 130.79 (114.40) µm from the anterior end, and one to two annules were posterior to the hemizonid (Fig. 4G). There was a lateral field with four incisures (Figs. 1D, 4G). The dorsal gland

Eggs

Body hyaline without any markings was presented; juveniles folded six times (Fig. 3F).

Male

The male was not found.

Type material

Holotype and paratype material (20 cysts, 20 females, and 20 second-stage juveniles) were deposited in the nematode collection of the Department of Plant Protection, Biocontrol Engineering Laboratory of Crop Diseases and Pests of Gansu Province, Lanzhou, China.

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Table 1. Morphometrics of H. microulae sp. n.

  • Stage
  • Character
  • Holotype
  • Paratype

Cyst

n

20
L (excluding length) Diam.
521.79 419.33
1.27
495.50 41.01 (413.93-543.23) 384.29 43.30 (304.96-455.51)

  • 1.30 0.09 (1.12-1.45)
  • L/Diam

Fenestral length Fenestral width Vulval slit length
30.72 36.16 35.53
31.14 1.36 (28.33-32.78) 37.75 1.61 (35.46-40.07) 39.00 2.78 (35.16-44.38)
Female

n

20
Length Width
454.21 28.32 (381.62-496.48) 326.47 31.42 (256.32-421.63)

  • 1.40 0.12 (1.28-1.56)
  • Length/width

Second-stage juveniles

n

20

  • Body length
  • 567.73 43.24 (505.62-627.92)

23.19 1.31 (20.39-25.43) 24.54 1.34 (21.97-27.67)
4.37 0.33 (3.91-5.00)
10.07 1.18 (8.56-12.52)
4.26 0.33 (3.63-4.90) 4.63 0.44 (3.90-5.50)
11.07 0.82 (9.65-12.75)
25.73 1.21 (24.07-28.92)
2.53 0.33 (2.04-3.19) 5.30 0.54 (4.39-6.09)
85.57 5.02 (76.37-95.26)
5.13 0.72 (4.03-6.41)
Body width at mid-body

abc

c′

Lip-region height Lip-region diam. Stylet length Stylet base height Stylet base width Median bulb from the anterior end (MB) Opening of dorsal pharyngeal gland from the stylet base (DGO)

  • Excretory pore from the anterior end (EP)
  • 114.40 6.89 (102.46-130.79)

12.33 1.49 (10.51-15.82) 13.23 1.00 (11.24-15.26) 56.67 3.75 (48.90-60.80) 28.63 1.91 (24.29-30.60)
6.65 0.37 (5.76-7.53)
Median bulb width (MBW) Diam. at the anus Tail length Hyaline portion tail L/MB

  • TL/H
  • 1.98 0.10 (1.64-2.08)

Egg

n

20
Length Width
111.61 8.02 (100.21-124.65)
50.34 6.71 (35.64-71.51)

  • 2.26 0.38 (1.43-3.26)
  • Length/width

Note: All measurements are in µm, and in the form: mean standard (range).

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47µm), longer J2s body length (568µm vs 422µm), stylet knobs rounded and flat or slightly concave anteriorly vs concave anterior face, higher MB value (86µm vs 66µm), longer excretory pore distance from the anterior end (114µm vs 99µm), and longer tail length (57µm vs 52µm).
The new species differs from H. cruciferae by having a bigger size of cysts (495×384µm vs 429×333µm), slightly shorter fenestral length (31µm vs 34µm), shorter vulval length (39µm vs 45µm), longer J2s body length (568µm vs 431µm), higher MB value (86µm vs 68µm), longer excretory pore distance from the anterior end (114µm vs 101µm), longer tail length (57µm vs 50µm), and longer length of hyaline tail portion (29µm vs 25µm).
The new species differs from H. persica by a shorter fenestral length (31µm vs 47µm), absence of bullae (vs present), shorter vulval slit length (39µm vs 49µm), longer J2s body length (568µm vs 440µm), stylet knobs (flat or concave anteriorly vs projecting slightly anteriorly, convex posteriorly), longer stylet (26µm vs 23µm), higher MB value (86µm vs 70µm), longer excretory pore distance from the anterior end (114µm vs 103µm), longer tail length (57µm vs 47µm), and longer length of hyaline tail portion (29µm vs 24µm).
Compared with H. urticae, the new species has a smaller size of cysts (495×384µm vs 492×435µm), vulval cone obtrusive (vs unobtrusive) and absence of egg sac (vs presence), shorter fenestral length (31µm vs 38µm), shorter vulval slit length (39µm vs 46µm), longer J2s body length (568µm vs 541µm), shorter DGO (8µm vs 5µm), and shorter excretory pore distance from the anterior end (114µm vs 130µm).
The new species differs from H. circeae having a smaller size of cysts (495×384µm vs 555×397µm), a shorter fenestral length (31µm vs 43µm), vulval slit length (39µm vs 48µm), longer J2s body length (568µm vs 434µm), stylet knobs (rounded and slightly sloping posteriorly vs rounded and flat or slightly concave anteriorly), higher MB value (86µm vs 70µm), longer excretory pore distance from the anterior end (114µm vs 101µm), longer tail length (57µm vs 52µm), and longer length of hyaline tail portion (29µm vs 26µm).

Type host and locality

Heterodera microulae sp. n. was collected from the roots and rhizosphere soil of Microula sikkimensis

Hemsl. (Boraginaceae, Tubiflorae, Metachlamydeae)

in Tianzhu county of Gansu Province, China. The geographical position is N 37°1146 ; E 102°47 6 . This site was located in continental highland with the vegetation type of meadow grassland and the soil is composed of chernozems. The climatic parameters of the site include 450mm of average rainfall and an approximate −2 air temperature.

  • ′
  • ″
  • ′ ″

Etymology

The species is named after the host of its isolation.

Diagnosis and relationships

Heterodera microulae sp. n. is characterized by having lemon-shaped cysts that have protruding necks and obtuse vulval cones. The cysts are 414 to 543-µm long and 305 to 456-µm wide having ambifenestrate vulval cone and bullae are absent. Females are white in color with a subcrystalline layer. Second-stage juveniles are straight or slightly curved ventrally with four incisures in the lateral field. The juveniles are 506 to 628-µm long having strong stylets with welldeveloped rounded stylet knobs, genital primordium situated at 59 to 62% of body length, and tail 49 to 61-µm long with a hyaline portion of 24 to 33µm. Eggs are hyaline without any markings; juveniles inside the eggs form sixfold.
The new species belongs to the Goettingiana group of Heterodera; currently, the group contains seven valid species, viz, Heterodera goettingiana (Liebscher, 1892), H. carotae (Jones, 1950), H. cruciferae (Franklin, 1945), H. circeae (Subbotin and Turhan, 2004), H. scutellariae (Subbotin and Turhan, 2004), H. urticae (Cooper, 1955), and H. persica (Maafi et al., 2006).
The new species differs from H. goettingiana by having a shorter fenestral length (31µm vs 35µm), absence of bullae (vs few), weak underbridge (vs 117µm), longer J2s body length (568µm vs 486µm), stylet knobs rounded and flat or slightly concave anteriorly vs smoothly rounded to slightly hookshaped with a recurved anterior surface, longer distance of median bulb from the anterior end (MB) (86µm vs 70µm), shorter excretory pore distance from the anterior end (114µm vs 158µm), and shorter length of hyaline tail portion (29µm vs 37µm).
The new species differs from H. scutellariae, having smaller cysts (495×384µm vs 560×424µm), by a shorter fenestral length (31µm vs 35µm), vulval slit length (39µm vs 43µm), longer J2s body length (568µm vs 408µm), higher MB value (86µm vs 62µm), longer excretory pore distance from the anterior end (114µm vs 89µm), longer tail length (57µm vs 47µm), and longer length of hyaline tail portion (29µm vs 25µm).
The new species is differentiated from H. carotae by having a bigger size of cysts (495×384µm vs 408×309µm), shorter vulval slit length (39µm vs

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    Nematology Circular No. 221 Fl. Dept. Agriculture & Cons. Svcs. November 2002 Division of Plant Industry The Mediterranean Cereal Cyst Nematode, Heterodera latipons: a Menace to Cool Season Cereals of the United States1 N. Greco2, N. Vovlas2, A. Troccoli2 and R.N. Inserra3 INTRODUCTION: Cool season cereals, such as hard and bread wheat, oats and barley, are among the major staple crops of economic importance worldwide. These monocots are parasitized by many pathogens and pests including plant parasitic nematodes. Among nematodes, cyst-forming nematodes (Heterodera spp.) are considered to be very damaging because of crop losses they induce and their worldwide distribution. The most economically important cereal cyst nematode species damaging winter cereals are: Heterodera avenae Wollenweber, which occurs in the United States and is the most widespread and damaging on a world basis; H. filipjevi (Madzhidov) Stelter, found in Europe and Mediterranean areas and most often confused with H. avenae; and H. hordecalis Andersson, which seems to be confined to central and north European countries. In the 1950s and early 1960s, a cyst nematode was detected in the Mediterranean region (Israel and Libya) on the roots of stunted wheat plants (Fig. 1 A,B). It was described as a new species and named H. latipons based on morphological characteristics of the Israel population (Franklin 1969). Subsequently, damage by H. latipons was reported on cereals in other Mediterranean countries (Fig. 1). MORPHOLOGICAL CHARACTERISTICS AND DIAGNOSIS: Heterodera latipons cysts are typically ovoid to lemon-shaped as those of H. avenae. They belong to the H. avenae group be- cause they have short vulva slits (< 16 µm) (Figs.
  • JOURNAL of NEMATOLOGY Morphological And

    JOURNAL of NEMATOLOGY Morphological And

    JOURNAL OF NEMATOLOGY Article | DOI: 10.21307/jofnem-2020-098 e2020-98 | Vol. 52 Morphological and molecular characterization of Heterodera dunensis n. sp. (Nematoda: Heteroderidae) from Gran Canaria, Canary Islands Phougeishangbam Rolish Singh1,2,*, Gerrit Karssen1, 2, Marjolein Couvreur1 and Wim Bert1 Abstract 1Nematology Research Unit, Heterodera dunensis n. sp. from the coastal dunes of Gran Canaria, Department of Biology, Ghent Canary Islands, is described. This new species belongs to the University, K.L. Ledeganckstraat Schachtii group of Heterodera with ambifenestrate fenestration, 35, 9000, Ghent, Belgium. presence of prominent bullae, and a strong underbridge of cysts. It is characterized by vermiform second-stage juveniles having a slightly 2National Plant Protection offset, dome-shaped labial region with three annuli, four lateral lines, Organization, Wageningen a relatively long stylet (27-31 µm), short tail (35-45 µm), and 46 to 51% Nematode Collection, P.O. Box of tail as hyaline portion. Males were not found in the type population. 9102, 6700, HC, Wageningen, Phylogenetic trees inferred from D2-D3 of 28S, partial ITS, and 18S The Netherlands. of ribosomal DNA and COI of mitochondrial DNA sequences indicate *E-mail: PhougeishangbamRolish. a position in the ‘Schachtii clade’. [email protected] This paper was edited by Keywords Zafar Ahmad Handoo. 18S, 28S, Canary Islands, COI, Cyst nematode, ITS, Gran Canaria, Heterodera dunensis, Plant-parasitic nematodes, Schachtii, Received for publication Systematics, Taxonomy. September
  • "Structure, Function and Evolution of the Nematode Genome"

    "Structure, Function and Evolution of the Nematode Genome"

    Structure, Function and Advanced article Evolution of The Article Contents . Introduction Nematode Genome . Main Text Online posting date: 15th February 2013 Christian Ro¨delsperger, Max Planck Institute for Developmental Biology, Tuebingen, Germany Adrian Streit, Max Planck Institute for Developmental Biology, Tuebingen, Germany Ralf J Sommer, Max Planck Institute for Developmental Biology, Tuebingen, Germany In the past few years, an increasing number of draft gen- numerous variations. In some instances, multiple alter- ome sequences of multiple free-living and parasitic native forms for particular developmental stages exist, nematodes have been published. Although nematode most notably dauer juveniles, an alternative third juvenile genomes vary in size within an order of magnitude, com- stage capable of surviving long periods of starvation and other adverse conditions. Some or all stages can be para- pared with mammalian genomes, they are all very small. sitic (Anderson, 2000; Community; Eckert et al., 2005; Nevertheless, nematodes possess only marginally fewer Riddle et al., 1997). The minimal generation times and the genes than mammals do. Nematode genomes are very life expectancies vary greatly among nematodes and range compact and therefore form a highly attractive system for from a few days to several years. comparative studies of genome structure and evolution. Among the nematodes, numerous parasites of plants and Strikingly, approximately one-third of the genes in every animals, including man are of great medical and economic sequenced nematode genome has no recognisable importance (Lee, 2002). From phylogenetic analyses, it can homologues outside their genus. One observes high rates be concluded that parasitic life styles evolved at least seven of gene losses and gains, among them numerous examples times independently within the nematodes (four times with of gene acquisition by horizontal gene transfer.
  • Rapid Pest Risk Analysis (PRA) For: Stage 1: Initiation

    Rapid Pest Risk Analysis (PRA) For: Stage 1: Initiation

    Rapid Pest Risk Analysis (PRA) for: Globodera tabacum s.I. November 2014 Stage 1: Initiation 1. What is the name of the pest? Preferred scientific name: Globodera tabacum s.l. (Lownsbery & Lownsbery, 1954) Skarbilovich, 1959 Other scientific names: Globodera tabacum solanacearum (Miller & Gray, 1972) Behrens, 1975 syn. Heterodera solanacearum Miller & Gray, 1972 Heterodera tabacum solanacearum Miller & Gray, 1972 (Stone, 1983) Globodera Solanacearum (Miller & Gray, 1972) Behrens, 1975 Globodera Solanacearum (Miller & Gray, 1972) Mulvey & Stone, 1976 Globodera tabacum tabacum (Lownsbery & Lownsbery, 1954) Skarbilovich, 1959 syn. Heterodera tabacum Lownsbery & Lownsbery, 1954 Globodera tabacum (Lownsbery & Lownsbery, 1954) Behrens, 1975 Globodera tabacum (Lownsbery & Lownsbery, 1954) Mulvey & Stone, 1976 Globodera tabacum virginiae (Miller & Gray, 1968) Stone, 1983 syn. Heterodera virginiae Miller & Gray, 1968 Heterodera tabacum virginiae Miller & Gray, 1968 (Stone, 1983) Globodera virginiae (Miller & Gray, 1968) Stone, 1983 Globodera virginiae (Miller & Gray, 1968) Behrens, 1975 Globodera virginiae (Miller & Gray, 1968) Mulvey & Stone, 1976 Preferred common name: tobacco cyst nematode 1 This PRA has been undertaken on G. tabacum s.l. because of the difficulties in separating the subspecies. Further detail is given below. After the description of H. tabacum, two other similar cyst nematodes, colloquially referred to as horsenettle cyst nematode and Osbourne's cyst nematode, were later designated by Miller et al. (1962) from Virginia, USA. These cyst nematodes were fully described and named as H. virginiae and H. solanacearum by Miller & Gray (1972), respectively. The type host for these species was Solanum carolinense L.; other hosts included different species of Nicotiana, Physalis and Solanum, as well as Atropa belladonna L., Hycoscyamus niger L., but not S.
  • DNA Barcoding Evidence for the North American Presence of Alfalfa Cyst Nematode, Heterodera Medicaginis Tom Powers

    DNA Barcoding Evidence for the North American Presence of Alfalfa Cyst Nematode, Heterodera Medicaginis Tom Powers

    University of Nebraska - Lincoln DigitalCommons@University of Nebraska - Lincoln Papers in Plant Pathology Plant Pathology Department 8-4-2018 DNA barcoding evidence for the North American presence of alfalfa cyst nematode, Heterodera medicaginis Tom Powers Andrea Skantar Timothy Harris Rebecca Higgins Peter Mullin See next page for additional authors Follow this and additional works at: https://digitalcommons.unl.edu/plantpathpapers Part of the Other Plant Sciences Commons, Plant Biology Commons, and the Plant Pathology Commons This Article is brought to you for free and open access by the Plant Pathology Department at DigitalCommons@University of Nebraska - Lincoln. It has been accepted for inclusion in Papers in Plant Pathology by an authorized administrator of DigitalCommons@University of Nebraska - Lincoln. Authors Tom Powers, Andrea Skantar, Timothy Harris, Rebecca Higgins, Peter Mullin, Saad Hafez, Zafar Handoo, Tim Todd, and Kirsten S. Powers JOURNAL OF NEMATOLOGY Article | DOI: 10.21307/jofnem-2019-016 e2019-16 | Vol. 51 DNA barcoding evidence for the North American presence of alfalfa cyst nematode, Heterodera medicaginis Thomas Powers1,*, Andrea Skantar2, Tim Harris1, Rebecca Higgins1, Peter Mullin1, Saad Hafez3, Abstract 2 4 Zafar Handoo , Tim Todd & Specimens of Heterodera have been collected from alfalfa fields 1 Kirsten Powers in Kearny County, Kansas and Carbon County, Montana. DNA 1University of Nebraska-Lincoln, barcoding with the COI mitochondrial gene indicate that the species is Lincoln NE 68583-0722. not Heterodera glycines, soybean cyst nematode, H. schachtii, sugar beet cyst nematode, or H. trifolii, clover cyst nematode. Maximum 2 Mycology and Nematology Genetic likelihood phylogenetic trees show that the alfalfa specimens form a Diversity and Biology Laboratory sister clade most closely related to H.
  • Heterodera Glycines

    Heterodera Glycines

    Bulletin OEPP/EPPO Bulletin (2018) 48 (1), 64–77 ISSN 0250-8052. DOI: 10.1111/epp.12453 European and Mediterranean Plant Protection Organization Organisation Europe´enne et Me´diterrane´enne pour la Protection des Plantes PM 7/89 (2) Diagnostics Diagnostic PM 7/89 (2) Heterodera glycines Specific scope Specific approval and amendment This Standard describes a diagnostic protocol for Approved in 2008–09. Heterodera glycines.1 Revision approved in 2017–11. This Standard should be used in conjunction with PM 7/ 76 Use of EPPO diagnostic protocols. Terms used are those in the EPPO Pictorial Glossary of Morphological Terms in Nematology.2 (Niblack et al., 2002). Further information can be found in 1. Introduction the EPPO data sheet on H. glycines (EPPO/CABI, 1997). Heterodera glycines or ‘soybean cyst nematode’ is of major A flow diagram describing the diagnostic procedure for economic importance on Glycine max L. ‘soybean’. H. glycines is presented in Fig. 1. Heterodera glycines occurs in most countries of the world where soybean is produced. It is widely distributed in coun- 2. Identity tries with large areas cropped with soybean: the USA, Bra- zil, Argentina, the Republic of Korea, Iran, Canada and Name: Heterodera glycines Ichinohe, 1952 Russia. It has been also reported from Colombia, Indonesia, Synonyms: none North Korea, Bolivia, India, Italy, Iran, Paraguay and Thai- Taxonomic position: Nematoda: Tylenchina3 Heteroderidae land (Baldwin & Mundo-Ocampo, 1991; Manachini, 2000; EPPO Code: HETDGL Riggs, 2004). Heterodera glycines occurs in 93.5% of the Phytosanitary categorization: EPPO A2 List no. 167 area where G. max L. is grown.
  • &lt;I&gt;Heterodera Glycines&lt;/I&gt; Ichinohe

    <I>Heterodera Glycines</I> Ichinohe

    University of Nebraska - Lincoln DigitalCommons@University of Nebraska - Lincoln Theses, Dissertations, and Student Research in Agronomy and Horticulture Agronomy and Horticulture Department Summer 8-5-2013 MULTIFACTORIAL ANALYSIS OF MORTALITY OF SOYBEAN CYST NEMATODE (Heterodera glycines Ichinohe) POPULATIONS IN SOYBEAN AND IN SOYBEAN FIELDS ANNUALLY ROTATED TO CORN IN NEBRASKA Oscar Perez-Hernandez University of Nebraska-Lincoln Follow this and additional works at: https://digitalcommons.unl.edu/agronhortdiss Part of the Plant Pathology Commons Perez-Hernandez, Oscar, "MULTIFACTORIAL ANALYSIS OF MORTALITY OF SOYBEAN CYST NEMATODE (Heterodera glycines Ichinohe) POPULATIONS IN SOYBEAN AND IN SOYBEAN FIELDS ANNUALLY ROTATED TO CORN IN NEBRASKA" (2013). Theses, Dissertations, and Student Research in Agronomy and Horticulture. 65. https://digitalcommons.unl.edu/agronhortdiss/65 This Article is brought to you for free and open access by the Agronomy and Horticulture Department at DigitalCommons@University of Nebraska - Lincoln. It has been accepted for inclusion in Theses, Dissertations, and Student Research in Agronomy and Horticulture by an authorized administrator of DigitalCommons@University of Nebraska - Lincoln. MULTIFACTORIAL ANALYSIS OF MORTALITY OF SOYBEAN CYST NEMATODE (Heterodera glycines Ichinohe) POPULATIONS IN SOYBEAN AND IN SOYBEAN FIELDS ANNUALLY ROTATED TO CORN IN NEBRASKA by Oscar Pérez-Hernández A DISSERTATION Presented to the Faculty of The graduate College at the University of Nebraska In Partial Fulfillment of Requirements For the Degree of Doctor of Philosophy Major: Agronomy (Plant Pathology) Under the Supervision of Professor Loren J. Giesler Lincoln, Nebraska August, 2013 MULTIFACTORIAL ANALYSIS OF MORTALITY OF SOYBEAN CYST NEMATODE (Heterodera glycines Ichinohe) POPULATIONS IN SOYBEAN AND IN SOYBEAN FIELDS ANNUALLY ROTATED TO CORN IN NEBRASKA Oscar Pérez-Hernández, Ph.D.
  • Weed Risk Assessment for Torilis Leptophylla (L.) Rchb. F. (Apiaceae)

    Weed Risk Assessment for Torilis Leptophylla (L.) Rchb. F. (Apiaceae)

    Weed Risk Assessment for Torilis United States leptophylla (L.) Rchb. f. (Apiaceae) – Department of Bristlefruit hedgeparsley Agriculture Animal and Plant Health Inspection Service March 22, 2017 Version 1 Left: Herbarium sample of the inflorescence of T. leptophylla [image obtained from the Missouri Botanical Garden under CC-BY-NC-SA 3.0 (MBG, 2017)]. Right: Detailed drawing of the fruit showing the barbs at the end of the spines (source: Reed, 1977). Agency Contact: Plant Epidemiology and Risk Analysis Laboratory Center for Plant Health Science and Technology Plant Protection and Quarantine Animal and Plant Health Inspection Service United States Department of Agriculture 1730 Varsity Drive, Suite 300 Raleigh, NC 27606 Weed Risk Assessment for Torilis leptophylla Introduction Plant Protection and Quarantine (PPQ) regulates noxious weeds under the authority of the Plant Protection Act (7 U.S.C. § 7701-7786, 2000) and the Federal Seed Act (7 U.S.C. § 1581-1610, 1939). A noxious weed is defined as “any plant or plant product that can directly or indirectly injure or cause damage to crops (including nursery stock or plant products), livestock, poultry, or other interests of agriculture, irrigation, navigation, the natural resources of the United States, the public health, or the environment” (7 U.S.C. § 7701-7786, 2000). We use the PPQ weed risk assessment (WRA) process (PPQ, 2015) to evaluate the risk potential of plants, including those newly detected in the United States, those proposed for import, and those emerging as weeds elsewhere in the world. The PPQ WRA process includes three analytical components that together describe the risk profile of a plant species (risk potential, uncertainty, and geographic potential; PPQ, 2015).